B RA I N RE SE A R CH RE V I EW S 57 ( 20 0 8 ) 1 2 51 3 3

a v a i l a b l e a t w w w. s c i e n c e d i r e c t . c o m

w w w. e l s e v i e r. c o m / l o c a t e / b r a i n r e s r e v

Review

Combining modules for movement

E. Bizzia,, V.C.K. Cheungb , A. d'Avellac , P. Saltiela , M. Treschd

a
Department of Brain and Cognitive Sciences and McGovern Institute for Brain Research, Massachusetts Institute of Technolgy 46-6189,
77 Massachusetts Avenue, Cambridge, MA 02139, USA
b
Division of Health Sciences and Technology, Harvard Medical School and Massachusetts Institute of Technology, USA
c
Department of Neuromotor Physiology, Instituto di Ricovero e Cura a Carattere Scientifico, Foundazione Santa Lucia, Italy
d
Department of Biomedical Engineering, Northwestern University and Rehabilitation Institute of Chicago, USA

A R T I C LE I N FO AB S T R A C T

Article history: We review experiments supporting the hypothesis that the vertebrate motor system
Accepted 4 August 2007 produces movements by combining a small number of units of motor output. Using a variety
Available online 5 September 2007 of approaches such as microstimulation of the spinal cord, NMDA iontophoresis, and an
examination of natural behaviors in intact and deafferented animals we have provided
Keywords: evidence for a modular organization of the spinal cord. A module is a functional unit in the
Modular organization spinal cord that generates a specific motor output by imposing a specific pattern of muscle
Spinal cord activation. Such an organization might help to simplify the production of movements by
Muscle synergies reducing the degrees of freedom that need to be specified.
Factorization algorithms 2007 Elsevier B.V. All rights reserved.

Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125
2. The construction of movements with muscle synergies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
3. Muscle synergies extracted from intact, freely moving frogs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 128
4. Muscle synergies extracted from deafferented frogs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132

1. Introduction

In the natural world, some complex systems are discrete
combinatorial systemsthey utilize a finite number of discrete
elements to create larger structures. The genetic code, lan-
guage and perceptual phenomena are examples of systems in
which discrete elements and a set of rules can generate a large
number of meaningful entities that are quite distinct from
those of their elements. A question of considerable importance
is whether this fundamental characteristic of language and
genetics is also a feature of other biological systems. In par-
ticular, whether the activity of the vertebrate motor system,

Corresponding author.
E-mail address: ebizzi@mit.edu (E. Bizzi).

0165-0173/$ see front matter 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.brainresrev.2007.08.004
126 B RA I N R E SE A R CH RE V I EW S 57 ( 20 0 8 ) 1 2 51 3 3
with its impressive capacity to find original motor solutions to
an infinite set of ever changing circumstances, results from the
combinations of discrete elements.
The ease with which we move hides the complexity
inherent in the execution of even the simplest tasks. Even
movements we make effortlessly, such as reaching for an
object, involve the activation of many thousands of motor
units in numerous muscles. Given this large number of degrees
of freedom of the motor system we, as well as a number of
investigators, have put forward the hypothesis that the CNS
handles this large space with a hierarchical architecture based
upon the utilization of discrete building blocks whose combi-
nations result in the construction of a variety of different
movements (Arbib, 1981; Tsetlin, 1973). In particular, investi-
gators influenced by the AI perspective on the control of
complex systems have argued for a hierarchical decomposi-
tion with modules, or building blocks, as the most effective
way to select a control signal from a large search space (Russell
and Norvig, 1995).
In the last few years, my colleagues and I have asked a
specific question: are there simple units that can be flexibly
combined to accomplish a variety of motor tasks? We have
addressed this fundamental and long-standing question in
experiments that utilize spinalized frogs (Bizzi et al., 1991;
Giszter et al., 1993),freely moving frogs (d'Avella et al., 2003)
and rats (Tresch and Bizzi, 1999). With an array of approaches
such as microstimulation of the spinal cord, NMDA iontopho-
resis, and an examination of natural behaviors in intact and
deafferented animals we have provided evidence for a mod-
ular organization of the frog's and rat's spinal cord. A module
is a functional unit in the spinal cord that generates a specific
motor output by imposing a specific pattern of muscle ac-
tivation. Such patterns, in which a group of muscles are
activated in a fixed balance, have previously been considered
as muscle synergies. Other investigators have generated
corroborative evidence in cats (Lemay et al., 2001; Ting and
Macpherson, 2005; Krouchev et al., 2006). A clear-cut example
of a recombination of synergies is from locomotion with the
different limb CPGs. Each CPG can operate independently, but
the four limb CPG can also be combined in different patterns as
in a walk, a trot or a gallop (Grillner, 1981, Handbook chapter).
Based on extensive indirect evidence, Grillner suggested that
each limb CPG can be further subdivided into unit CPGs
controlling synergist muscles acting at each joint (Grillner,
1981, 1985). It has also been proposed that these different unit
CPGs synergies can be the independent target for the
supraspinal commands used to design different volitional
movements involving a limited set of joints (Grillner, 1985,
2006; Grillner and Zangger, 1979).
The output of a module can be characterized as a force field.
A force field is a mapping that associates each position of the
frog's hindlimb with a corresponding force generated by the
neuromuscular system. Force-fields have been measured by
placing the frog's ankle in different locations in the leg's
workspace and recording at each location the response to
microstimulation of the same site in the spinal cord. The
majority of force fields generated by stimulation of different
areas of the lumbar gray were found to converge toward an
equilibrium point. In addition, the force fields could be grouped
into a few classes (Bizzi et al., 1991; Giszter et al., 1993).
Our results have shown that not only the electrical but also
the chemical stimulation (NMDA) of the premotor neuronal
circuitry of the spinal cord imposes a specific balance of muscle
activation leading to a convergent force field (CFF). In addition,
in a series of control experiments, we have shown that this
pattern of forces is not the result of current spread or random
activation of the motor neurons. Neither can it result from
activating the fibers of passage of the descending fibers and
those of the sensory systems. On the basis of these results
(Giszter et al., 1993; Saltiel et al., 2001), we have concluded that
distinct interneuronal networks of the spinal cord must be the
source of specific types of CFFs.
Another observation derived from microstimulation of the
frog's and the rat's spinal cord is that the fields induced by
the focal activation of the cord follow the principle of vector
summation. Bizzi et al. (1991), Mussa-Ivaldi et al. (1994), and
more recently, Lemay et al. (2001) have shown that the si-
multaneous stimulation of two sites, each generating a
different force field, results in the vector sum of the two fields
in most instances. When the pattern of forces recorded at the
ankle following co-stimulation were compared with those
computed by summation of the two individual fields, Mussa-
Ivaldi et al. (1994) found that the co-stimulation fields and the
summation fields were equivalent in more than 87% of cases.
Similar results have been obtained by Tresch and Bizzi (1999)
by stimulating the spinal cord of the rat. Recently, Kargo and
Giszter (2000) showed that force field summation underlies the
control of limb trajectories in the frog.
Vector summation of force fields implies that the complex
non-linearities that characterize the interactions both among
neurons and between neurons and muscles are in some
way eliminated. More importantly, this result has lead to a
novel hypothesis for explaining movement and posture
based on combinations of few modules. These modules may
be viewed as representing an elementary alphabet from
which, through superimposition, a vast number of actions
could be fashioned by impulses conveyed by supraspinal
pathways, and/or by the reflex pathways. Through computa-
tional analysis, Mussa-Ivaldi and Giszter (1992) and Mussa-
Ivaldi (1997) verified that this view of generation of movement
and posture has the competence for controlling a wide
repertoire of movements.
Recently, our laboratory has developed a novel method
to identify muscle synergies with help of a computational
analysis. This approach was first used by Tresch et al.
(1999) who described the muscle activation patterns evoked
from cutaneous stimulation of the hind limb in spinalized
frogs.
Tresch et al. (1999) showed that the motor response evoked
from cutaneous stimulation of a particular site on the hindlimb
resulted from the weighted combination of a few muscle
synergies. By changing the relative weighting of each of the
synergies depending on the site of cutaneous stimulation, the
nervous system could produce a range of different motor
responses.
Also of particular interest is the fact that Tresch et al. (1999)
compared the distinct muscle synergies derived from cutane-
ous stimulation with the patterns of muscle activation evoked
by microstimulation of the frog spinal cord (the force fields
identified by our previous research). Tresch found that the two
 B RA I N RE SE A R CH RE V I EW S 57 ( 20 0 8 ) 1 2 51 3 3
sets of EMG responses were very similar to one another. In
addition, the synergies evoked by NMDA were found by Saltiel
et al. (2001) to be qualitatively similar to those described by
Tresch.
2. The construction of movements with
muscle synergies
For a long time, investigators have recognized that one of the
basic questions in motor performance is whether the cortical
motor areas control individual muscles or make use of
synergistically linked group of muscles (Lee, 1984; Macpher-
son, 1991). Given that no natural movement involves just one
muscle, any motor act, a fortiori, involves a muscle synergy,
the question then has been whether the synergistic activation
of muscles derives from a fixed common neural drive or
is merely a phenomenological event of a given motor
coordination.
Despite the history of this issue, the vast literature on this
question indicates little consensus either for fixed synergies or
for individual control of muscles. For instance, Howard et al.
(1986) showed that the synergists around the elbow joint do not
co-vary under all conditions because the relationship between
the muscles varies with the nature of the task. Buchanan et al.
(1986) reached the same conclusion in experiments in which
subjects moved their arm in different directions. Along similar
lines (Hepp-Reymond et al., 1983) in an investigation of
isometric precision grip in the monkey found that muscles
that appeared correlated at one level of force were not nec-
essarily so at higher force levels. This observation was in-
terpreted as a lack of amplitude scaling and not in keeping with
idea of synergies.
The studies mentioned above as well as many others (see
Macpherson, 1991) are not in agreement with other reports
claiming that human postural responses are indeed organized
synergistically (Nashner, 1977; Crenna et al., 1987; McCollum
et al., 1984; Nashner and McCollum, 1985). However, the
synergies described by these investigators were present only
in restricted set of movements such as postural sways in the
sagittal plane, and further examination by others of more
complex postural responses showed different and richer
combinations of muscle activations.
Even though most investigators doubt the existence of fixed
synergies, they are nevertheless reluctant to accept the idea
that a separate control signal must be computed for each
muscle to achieve the appropriate movement. Various alter-
native mechanisms have been suggested such as hierarchical
control (Saltzman, 1979; Bullock and Grossberg, 1988; Das and
McCollum, 1988). According to these investigators, there is a
hierarchy of parameters or strategies that are controlled in any
motor act. Once the strategy is chosen a coordinated pattern of
muscle activity is selected, but the muscle groupings are not
considered to be fixedthey are formed and reformed each
time.
Summing up, there is little doubt that the issue of muscle
synergies has remained unsettled. However, there is a reason
for this predicamentthe approaches that have been used to
investigate this issue have been based on correlation methods,
which in this case are less than ideal for settling the muscle
127
synergy question. The recent introduction of novel computa-
tional procedures has opened a different way to approach the
issue of synergies. In 1999, Tresch and collaborators developed
a variety of essentially similar computational methods to
extract synergies from the recorded muscle activations. In
general, these methods try to decompose the observed muscle
patterns as simultaneous combinations of a number of
synergies. This decomposition is obtained using iterative
algorithms that are initialized with a set of arbitrary synergies.
The non-negative weighting coefficients of these arbitrary
synergies that best predict each response are then found. The
synergies are then updated by minimizing the error between
the observed response and the predicted response. This
process is then iterated until the algorithm converges on a
particular set of synergies. The algorithm extracts both a set of
synergies and the weighting coefficients of each synergy used
to reconstruct the EMG responses.
To explain why the computational method provides a
different perspective from the one afforded by the correlation
method, let us assume that a given muscle belongs to more
than one synergy. According to the correlation method, two
muscles, say, X and Y, are considered part of a same syn-
ergy, A, if they both scale in amplitude when more force
output is required during a task. A potential problem with
this approach may surface if, for example, muscle Y is
also found in synergy, B. Then, when synergies A and B
are recruited together in different contexts, the amplitude
scaling for X and Y might be different, and then the false
conclusion could be reached that no synergy between X and
Y exists.
Note that there are a number of factorization algorithms to
assess the hypothesis that motor behavior might be produced
through a combination of a small number of synergies. Tresch
et al. (2006) have compared different algorithms and found
that in general, most of the algorithms used to identify muscle
synergies perform comparably. In particular, non-negative
matrix factorization, independent component analysis, and
factor analysis performed at similar levels to one another.
When Tresch et al. (2006) applied these methods to experi-
mentally obtained data set, the best performing algorithms
identified synergies very similar to one another. These results
suggest that the muscle synergies found by a particular
algorithm are not an artifact of that algorithm, but reflect
basic aspects of muscle activation.
Finally, the synergistic link in a group of muscles might be
more general than the specific amplitude ratios among the
instantaneous activations of the muscles expressed by the
components extracted by factorization algorithms such FA,
ICA, and NMF. The coordination among muscle recruitments
expressed by a synergy might also be extended to the temporal
domain. This idea has led to the introduction of a novel
factorization algorithm (d'Avella and Tresch, 2002) to extract
time-varying synergies, i.e. the coordinated activations of
groups of muscles with specific time-varying profiles. Time-
varying synergies can naturally capture specific asynchronous
activations of groups of muscles and provide a parsimonious
model for the generation of muscle patterns. In fact, once the
synergies are specified, one amplitude scaling coefficient and
one time delay coefficient per synergies are sufficient for
generating a muscle pattern. In contrast, the entire time-
128 B RA I N R E SE A R CH RE V I EW S 57 ( 20 0 8 ) 1 2 51 3 3

course of the weighting coefficients is required with synchro-
nous synergies.
3. Muscle synergies extracted from intact,
freely moving frogs
The above experiments suggest that motor behavior might be
produced through the flexible combination of muscle syner-
gies. However, to more directly assess the utility of this
hypothesis, it is necessary to test its applicability to natural
behaviors. In recent experiments we have evaluated this issue
by examining several motor behaviors in intact, freely moving
frogs. We recorded simultaneously from a large number of
hindlimb muscles during locomotion, swimming, jumping and
defensive reflexes (d'Avella et al., 2003; d'Avella and Bizzi, 2005).
We extracted synergies from the pooled, rectified and
integrated EMGs records of thirteen leg muscles in 3 intact
frogs during swimming, jumping, and walking using a
computational analysis. An iterative algorithm was used to
decompose the muscle patterns as combination of time-
varying muscle synergies independently scaled in amplitude
and shifted in time. This iterative algorithm finds a set of
muscle synergies and, for each muscle pattern, the amplitude
and delay of each synergy that minimize the reconstruction
error for the entire dataset.
In Fig. 1 we show the five time-varying synergies extracted
from all the rectified, low-pass filtered, and integrated (10 ms)
EMGs recorded during a total of 2174 jumps, walking cycles, and
swimming cycles in 3 frogs. The five extracted synergies include
all 13 muscles. The first 3 synergies (W1, W2, and W3) recruit
mainly extensors while W4 and W5 recruit mainly flexors. The
most active muscles of synergy W1 are the hip extensors rectus
internus (RI), adductor magnus (AD), and semimembranosus
(SM), the knee extensor vastus internus (VI), and the ankle
extensors peroneus (PE) and gastrocnemius (GA). The most
active muscles of the synergy W2 are SM, vastus externus (VE),
and GA. In W3, RI, SM, and VI are the most active. The flexors
dominate synergy W4 with rectus anterior (RA), biceps (BI) and
ilio-psoas (IP). Synergy W5 mainly semitendinosus (ST) and IP.
Note that some of the muscles are present in more than one
synergylack of recognition of this fact has affected the inter-
pretation of amplitude scaling (Hepp-Reymond et al., 1983).
The R2 for the five synergies extracted from the entire data
set was 0.78. Thus a large fraction of the total variation of the
data was described by a model that has just 10 parameters (5
amplitude and 5 timing coefficients) once the synergies are
determined.

Fig. 1 Time-varying muscle synergies extracted from jumping, swimming, and walking muscle patterns in three frogs. Each
synergy (columns W1 to W5 ) represents the activation time-course (in color code) of 13 muscles over 30 samples (300 ms
total duration) normalized to the maximum sample of each muscle. (RI = rectus internus, AD = adductor magnus
SM = semimembranosus, VI = the knee extensor vastus internus, VE = vastus externus, RA = rectus anterior, PE = the ankle
extensors peroneus, GA = gastrocnemius, ST = mainly semitendinosus, SA = semitendinosus, BI = biceps, IP = ilio-psoas,
TA = tibialis anterior).
 B RA I N RE SE A R CH RE V I EW S 57 ( 20 0 8 ) 1 2 51 3 3 129

Fig. 2 Examples of reconstruction of EMG patterns as combinations of time-varying muscle synergies. The three columns are
examples of a jump, a walking cycle, and a swimming cycle. Upper section (EMGs): the thick line shows the reconstruction of
muscle patterns and the shaded area represents the rectified, filtered and integrated EMGs. Lower section (synergies): the
coefficients of the five synergies as the horizontal position (onset delay, ti) and the height (amplitude, ci) of a rectangle whose
width corresponds to the synergy duration. The shaded profile in each rectangle illustrates the averaged time-course of the
muscle activation waveforms of the corresponding synergy. Note the different amplitude scaling used in the three columns.

Fig. 2 shows the reconstruction of muscle patterns (recti-
fied, filtered, and integrated EMGs, thin line and shaded area) for
a jump, a cycle of walking, and one of swimming as
combinations of the five synergies of Fig. 1 (thick line). The
synergy's amplitude is shown as the height of the rectangles
below the EMGs, and the delay coefficients by their horizontal
position. The essential features of the three patterns are well
captured by scaling in amplitude and shifting in time the five
time-varying synergies. In jumping (first column) two of the
three extension synergies are active (W1 and W3) together with
the two flexion synergies (W4 and W5). In walking (second
column) synergies, one, three, and four appear again but their
amplitude balance and recruitment order are radically differ-
ent from jumpingW4 dominates in amplitude, while W1 and
W3 are relatively small, and the timing between W3 and W4 is
reversed. Swimming (third column), in contrast, is dominated
by W2 and to a lesser extent by W5.
The examples illustrated by Fig. 2 demonstrate two im-
portant points: (1) that the same synergies are found in dif-
ferent behaviors; and (2) that different behaviors may be
constructed by combining the same synergies with different
timing and amplitude.
Fig. 3 (upper row, A, B, and C) illustrates the coefficient of
synergies displayed in Fig. 1. In C note jumps of different
amplitude and the amplitude modulation of synergy W1. In the
second row, walking over a flat (D) surface is shown . In E, F,
and G, walking on a progressively steeper surface is displayed
(20%, 30%, and 40 % incline). This figure demonstrates
amplitude scaling of the synergies W1, W2, W3, and W4. The
third row (H and I) demonstrates two examples of swimming at
different speeds. In i, the higher speed is reached by adding
synergies W1 and W3 to fortify extension and W4 for flexion.
The examples illustrated in Figs. 2 and 3 address the
important question of whether the synergies extracted by our
computational procedure have biological standing. Clearly, a
certain number of criteria must be satisfied in order to validate
the extracted synergies. Chief among them, is the evidence of
amplitude scaling of a given synergy which is illustrated in Fig. 3
by the frog's walk on a progressively inclined surface (E, F, and G)
and the jumps in b and c. Along the same lines, deletion of a
130 B RA I N R E SE A R CH RE V I EW S 57 ( 20 0 8 ) 1 2 51 3 3

Fig. 3 Scaling of synergy recruitment in different frog behaviors. Each panel represents the recruitment of the five synergies of
Fig. 1 to generate either a jump (AC), or a walking cycle (D to G), or a swimming cycle (H and I).

given synergy (i.e. coefficient equal to zero) like in the example
(H) in which W1 is absent during low power swimming makes
the same point. Another compelling criterion is the presence of
the same synergy, with its own internal temporal structure, in
different behaviors as illustrated several times in Figs. 2 and 3.
In conclusion, the examples shown here indicate that
combining muscle synergies is a strategy that the CNS utilizes
for the construction of movements in the frog. Recent results
from the study of the muscle patterns during reaching in humans
(d'Avella et al., 2006) suggest that this is a general strategy used by
all vertebrates for simplifying the control of limb movements.
4. Muscle synergies extracted from
deafferented frogs
The results described in the previous section suggest that the
CNS generates diverse motor outputs by combining a small
number of muscle synergies. But the precise role of sensory
feedback in organizing and activating these synergies has
remained an open question. It is possible that each synergy is
completely specified by spinal and/or supraspinal networks.
Alternatively, synergies might arise as emergent properties of
the entire neuronal network comprising both central circuits
and feedback loops.
We have recently attempted to address the above question
by simultaneously recording EMGs from 13 hindlimb muscles
of the frog during locomotor behaviors before and after
ipsilateral deafferentation, the procedure of removing sensory
inflow into the CNS by severing dorsal roots (Cheung et al.,
2005). In this study, as an initial assessment of afferent roles in
synergy organization, we extracted synchronous muscle
synergies from the intact and deafferented data sets. More-
over, to rigorously compare intact and deafferented synergies,
we developed a novel NMF-based procedure that searches for
synergies by minimizing the reconstruction error for the data
 B RA I N RE SE A R CH RE V I EW S 57 ( 20 0 8 ) 1 2 51 3 3
Fig. 4 Muscle synergies underlying intact and deafferented locomotor behaviors. (A) Synchronous muscle synergies extracted from the pooled intact and deafferented jumping
data of one frog. Four of the five synergies (Sh1Sh4) were found to be shared between the intact and deafferented data sets, and one (Desp), specific to the deafferented data set.
The fact that most of the synergies were extracted as shared synergies suggest that, many locomotor synergies are centrally organized. Modified from Cheung et al. (2005).
(B, C) Reconstructing intact and deafferented jumping EMGs with synergies and their corresponding activation coefficients. The original EMG data (rectified, filtered, and
integrated) are shown in black lines, and the time-varying coefficients activating the synchronous synergies are shown below the EMGs. The reconstruction of the motor pattern
is superimposed onto the original EMGs. The colors composing the reconstruction match the colors of the coefficients such that the colors reflect the respective contribution of
each synergy to the reconstruction at each time point. Modified from Cheung et al. (2005).

131
132 B RA I N R E SE A R CH RE V I EW S 57 ( 20 0 8 ) 1 2 51 3 3
set pooling both the intact and deafferented data, and at the
same time, indicates whether a synergy is shared between the
two data sets, or specific to either of the data sets.
Fig. 4A shows five synchronous synergies extracted from
the intact and deafferented data of one frog during jumping.
Four of the five synergies (Sh1Sh4) were synergies shared
between the intact and deafferented data sets, and one (Desp),
as a deafferented-specific synergy (i.e., it contributes to the
reconstruction of only the deafferented data). These synergies
together describe the intact and deafferented jumping data
with R2 values of 90.6% and 90%, respectively. The fact that in
both data sets, a similarly large amount of data variation is
captured by these synergies indicates that the finding of shared
synergies is not the result of one data set being described better
than the other, or of both data sets being described poorly.
To illustrate how the synergies shown in Fig. 4A can be used
to reconstruct the EMG data, we show two examples of EMG
reconstruction for two jumps recorded before (Fig. 4B) and after
(Fig. 4C) deafferentation, respectively. Each jump is divided
into three phases a, b, and c for ease of inspection. We see
that, the EMG patterns of these two jumps are different. In
particular, the burst duration of the flexor muscles IP, TA, BI,
and SA during phases b and c were prolonged after deaf-
ferentation. But these differences are nicely captured by the
prolonged activations of synergies Sh3 (light blue) and Sh4
(green), both of which are shared between the intact and
deafferented data sets.
The examples in Fig. 4 together demonstrate two important
points: (1) Many synergies underlying natural locomotor
behaviors are robust neural structures encoded within spinal
and/or supraspinal networks. This is suggested by the result
that most of the synergies were found to be shared between the
intact and deafferented data sets (Fig. 4A). (2) Sensory afferent
modulates the activation patterns of a set of centrally organized
synergies. This is illustrated in Figs. 4B, C, which show how EMG
changes observed after deafferentation can be characterized as
alterations in the activation pattern of shared synergies.
In conclusion, in the above sections, we have provided both
experimental and analytical results suggesting that linear
combinations of a small number of muscle synergies may be a
strategy utilized by the CNS to generate diverse motor outputs.
Furthermore, most of the synergies used for generating
locomotor behaviors are centrally organized, but their activa-
tions might be modulated by sensory feedback so that the final
motor outputs can be adapted to the external environment.
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